View cells in the hippocampus and prefrontal cortex of macaques during virtual navigation

Abstract

Cells selectively activated by a particular view of an environment have been found in the primate hippocampus (HPC). Whether view cells are present in other brain areas, and how view selectivity interacts with other variables such as object features and place remain unclear. Here, we explore these issues by recording the responses of neurons in the HPC and the lateral prefrontal cortex (LPFC) of rhesus macaques performing a task in which they learn new context‐object associations while navigating a virtual environment using a joystick. We measured neuronal responses at different locations in a virtual maze where animals freely directed gaze to different regions of the visual scenes. We show that specific views containing task relevant objects selectively activated a proportion of HPC units, and an even higher proportion of LPFC units. Place selectivity was scarce and generally dependent on view. Many view cells were not affected by changing the object color or the context cue, two task relevant features. However, a small proportion of view cells showed selectivity for these two features. Our results show that during navigation in a virtual environment with complex and dynamic visual stimuli, view cells are found in both the HPC and the LPFC. View cells may have developed as a multiarea specialization in diurnal primates to encode the complexities and layouts of the environment through gaze exploration which ultimately enables building cognitive maps of space that guide navigation.

Hippocampal spatial view cells, place cells, and concept cells: View representations

“…10. Several papers (including several in this Special Issue) have highlighted the presence of hippocampal and related neurons in primates including humans that respond to views of scenes, and not to the place where the individual is located (Corrigan et al, 2023;Donoghue et al, 2023;Mao et al, 2021;Tan et al, 2021;Tsitsiklis et al, 2020;Yang et al, 2023;Zhu et al, 2023). This helps to establish the encoding of views as key to understanding hippocampal function in primates including humans (Rolls, 2023b).…”

“…Several contributions to the Special Issue of Hippocampus (2023) provide evidence that many primate hippocampal neurons respond to the location being viewed "out there," not the place where the individual is located (Corrigan et al, 2023;Rolls, 2023b;Wirth, 2023;Zhu et al, 2023). Complementary evidence is also available for humans, in that in another paper in this Special Issue of Hippocampus, it was found that significant numbers of spatial view cells but not a significant number of place cells were found in the medial temporal lobe in a VR navigation task to the remembered location in a scene of a Treasure Chest (Donoghue et al, 2023).…”

“…In a virtual reality (VR) navigation task, further evidence was found that many macaque hippocampal neurons responded to the location being viewed, and not the place where the individual was located (Corrigan et al, 2023). They were not able to determine what coordinate framework (allocentric or egocentric) was being used.…”

Using multi-task experiments to test principles of hippocampal function

“…In this special issue, several studies have continued the quest of understanding allocentric versus egocentric representation in the hippocampus and surrounding areas. In a study of monkeys performing a context-object association task in a virtual environment, a considerable number of view cells were found in the hippocampus that activated whenever the monkey viewed a left or right side corridor at either end of a central corridor, thus potentially representing particular views in an egocentric rather than an allocentric coordinate framework (Corrigan et al, 2023). In another study, egocentric tuning was found in deep layers of the lateral entorhinal cortex in rats (C. Wang et al, 2023), extending previous work demonstrating egocentric tuning in the superficial layers of the lateral entorhinal cortex (C. Wang et al, 2018) and in the retrosplenial cortex (Alexander et al, 2020).…”

A place with a view: A first‐person perspective in the hippocampal memory space

“…However, I propose that the main difference between rodents and primates lies in the way that visual stimuli are encoded in the hippocampus, with primate hippocampal encoding preserving some egocentric codes beyond retinotopic or head/body centered reference frames in visual and parietal cortices. Taking into account the persistence of egocentric signals referencing stimuli with respect to the self in the primate hippocampal complex (Corrigan et al, 2023;Yang et al, 2023), it appears that primates' hippocampal cells privilege a first person' viewer perspective which maintains some egocentric attributes rather than an allocentric perspective. Items can be represented in relationship with others, but this allocentric relationship stays anchored to the first person's perspective limited to the front facing FOV characteristic of primates.…”